急性盐度胁迫对缢蛏肠道菌群结构及功能的影响

张紫娟; 戴文芳; 薛清刚; 林志华

doi:10.12284/hyxb2023146

急性盐度胁迫对缢蛏肠道菌群结构及功能的影响

doi: 10.12284/hyxb2023146

张紫娟^1,,
戴文芳^{1, 2, ,},
薛清刚^{1, 2},
林志华^{1, 2}

1.
浙江万里学院生物与环境学院浙江省水产种质资源高效利用技术研究重点实验室，浙江宁波 315100
2.
浙江万里学院宁海海洋生物种业研究院，浙江宁海 315604

基金项目: 浙江省自然科学基金项目（LQ22C190005）；宁波市“泛3315计划”现代农业创新团队项目（2019−2023）；浙江省“生物工程”一流学科学生创新计划项目（CX2022032）。

详细信息

作者简介:
张紫娟（1998—），女，四川省宜宾市人，主要从事海洋贝类微生物生态学研究。E-mail：zhangzijuan927@163.com

通讯作者:
戴文芳，助理研究员，主要从事水产养殖病害微生态防控技术研究。E-mail：daiwenfang@zwu.edu.cn

中图分类号: Q938.8；P714⁺.5
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出版历程
- 收稿日期: 2023-04-06
- 修回日期: 2023-07-10
- 网络出版日期: 2023-10-31
- 刊出日期: 2023-11-30

Effects of acute salinity stress on the gut bacterial community structure and functional potentials of Sinonvacula constricta

Zhang Zijuan^1
,,
Dai Wenfang^{1, 2
, ,},
Xue Qinggang^{1, 2},
Lin Zhihua^{1, 2}

1.
Zhejiang Key Laboratory of Aquatic Germplasm Resource, College of Biological & Environmental Sciences, Zhejiang Wanli University, Ningbo 315100, China
2.
Ninghai Institute of Mariculture Breeding and Seed Industry, Zhejiang Wanli University, Ninghai 315604, China

摘要

摘要: 盐度是水产动物肠道微生物稳态的重要影响因子，其对水产动物的生长和健康有着重要影响。缢蛏（Sinonovacula constricta）是一种埋栖类的滩涂养殖贝类，常受到盐度波动的影响。然而，盐度是否对缢蛏肠道组织及其肠道菌群造成不利影响尚不清楚。为此，本研究设置了低盐（5）、正常盐度（20）和高盐（35）3个不同的盐度胁迫组，分别在胁迫前（正常盐度20，0 d）和胁迫15 d后收集缢蛏样品，利用组织病理学、16S rRNA高通量测序技术以及PICRUSt2工具对各处理组样品的肠道组织结构、菌群构成及其潜在功能进行比较分析。结果显示，15 d的急性盐度胁迫对缢蛏肠道组织造成了不同程度的损害，表现为细胞空泡、组织坏死和绒毛杂乱等。在所有组中共鉴定到712个细菌操作分类单元（OTUs），其中共有OTUs占细菌总数的6.2%。低盐和高盐胁迫下缢蛏肠道主要优势菌分别隶属于γ-变形菌纲（γ-Proteobacteria）和α-变形菌纲（α-Proteobacteria）。急性盐度胁迫改变了肠道细菌α-多样性，且在低盐组中物种丰富度最低。低盐和高盐胁迫下缢蛏肠道细菌群落结构均发生了显著改变（p < 0.002），同时伴随肠道菌群种间互作的降低。3种盐度胁迫下缢蛏肠道菌群组装的生态过程主要是确定性过程，而在低盐胁迫下其确定性过程有所降低。功能预测结果表明，急性盐度胁迫显著改变了缢蛏肠道菌群介导的营养物质和能量代谢等相关的功能通路丰度，而与免疫相关的功能通路丰度在高盐组中显著升高。本研究结果表明，急性盐度胁迫可引起缢蛏肠道发生病理损伤并伴随肠道菌群及其潜在功能的明显改变，这些改变可能影响缢蛏的健康。
- 缢蛏 /
- 急性盐胁迫 /
- 肠道菌群 /
- 功能预测 /
- 组织损伤
Abstract: Salinity is a crucial factor affecting the gut microbial homeostasis of aquatic animals, which has a significant impact on their growth and health. Sinonovacula constricta, a buried cultivated bivalve in mudflat, is frequently affected by salinity fluctuation. However, it remains unclear whether salinity has undesirable effects on the gut tissue and microbial community of S. constricta. To address these concerns, this study set up three different salinity stress groups: low salinity (5), normal salinity (20) and high salinity (35), with normal salinity 20 at 0 day as the control. Samples of S. constricta were collected before stress (i.e., normal salinity 20, 0 day) and after stress for 15 days, and were analyzed the differences in gut tissue structure, gut microbial compositions and potential functions via using the histopathology, 16S rRNA high-throughput sequencing technology and PICRUSt2. Simultaneously, the guts from S. constricta under normal salinity at 0 day were taken for comparative analysis. The results showed that the acute salinity stress for 15 days caused varying degrees of damage to the gut tissue structure of S. constricta, as observed by the cell vacuolation, tissue necrosis and villi clutter. A total of 712 bacterial OTUs were identified across all groups, among which the number of shared OTUs accounted for 6.2% of total OTUs. The dominant bacteria in the gut of S. constricta under low- and high- salinity stress belonged to γ-Proteobacteria and α-Proteobacteria, respectively. Acute salinity stress altered the α-diversity of gut bacterial community, with the lowest species richness under low salinity stress. The gut bacterial community structure of S. constricta changed significantly (p < 0.002) under both low- and high- salinity stress, accompanied by a decrease in the interspecific interactions of gut bacterial community. The ecological processes governing gut bacterial assembly of S. constricta was mainly deterministic under three salinity stresses, and this process decreased under the low salinity stress. Functional prediction results showed that acute salinity stress significantly varied the abundance of S. constricta gut bacterial-mediated nutrient and energy metabolism-related functional pathways, whereas the abundance of immune-related functional pathways significantly increased under high salinity stress. These findings suggest that acute salinity stress can cause pathological damage to the gut of S. constricta, accompanied by obvious change in gut bacterial communities and functional potentials, which could affect the health of S. constricta.
- Sinonvacula constricta /
- acute salinity stress /
- gut bacterial community /
- functional prediction /
- tissue damage

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图 1 3种盐度胁迫下缢蛏的肠组织切片

A. 放大倍数×200；B. 放大倍数×400。a. 基底膜；b. 肌层；c. 肠腔；d. 绒毛；e. 杯状细胞。实心箭头：绒毛杂乱、缺损；空心箭头：坏死；虚线箭头：基底膜剥离；黑色方框：空泡化

Fig. 1 Gut tissue sections from Sinonvacula constricta under three salinity stress

A. ×200 magnification; B. ×400 magnification. a. Basement membrane; b. muscle layers; c. gut lumen; d. gut villus; e. goblet cells. Solid filled arrow: cilia defects; hollow filled arrow: necrosis; dotted arrow: basement membrane stripped; square frame: vacuolation

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图 2 3种盐度胁迫下缢蛏肠道共有和特有的细菌OTU数韦恩图

Fig. 2 Venn diagram of the number of shared and unique gut bacterial OTUs in Sinonvacula constricta underthree salinity stress

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图 3 3种盐度胁迫下缢蛏肠道优势细菌门（变形菌门归类到纲）（a）和细菌属（b）的平均相对丰度变化

Fig. 3 Changes in the average relative abundances of dominant gut bacterial phyla (Proteobacteria is assigned to the class level) (a) and genus (b) in Sinonvacula constricta under three salinity stress

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图 4 3种盐度胁迫下缢蛏肠道细菌群落的α-多样性指数变化

不同字母表示组间存在显著差异（p < 0.05）

Fig. 4 Changes in the α-diversity indexes of gut bacterial communities in Sinonvacula constricta under three salinity stress

Different letters indicate significant differences (p < 0.05) among groups

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图 5 非度量多维尺度分析（NMDS）展示3种盐度胁迫下缢蛏肠道细菌群落的结构差异

Fig. 5 Non-metric multidimensional scaling analysis (NMDS) showing the difference in gut bacterial community structures among Sinonvacula constricta under three salinity stress

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图 6 3种盐度胁迫下缢蛏肠道细菌群落的拓扑特性参数变化

Fig. 6 Changes in the topological characteristics of gut bacterial communities in Sinonvacula constricta under three salinity stress

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图 7 3种盐度胁迫下缢蛏肠道细菌群落的生态过程差异

虚线表示两者同等重要。虚线以下的群落表示确定性过程控制群落组装，虚线以上的群落则表示随机性过程是主要的

Fig. 7 Difference of ecological processes of gut bacterial communities in Sinonvacula constricta under three salinity stress

The dashed line denotes equal roles for both. A community below the line indicates that determinism dominantly governs the community assembly, while a community above the line indicates that stochasticity is dominant

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图 8 热图展示3种盐度胁迫下缢蛏肠道细菌群落潜在功能途径的丰度（平方根转换）分布变化

热图中颜色从蓝到红代表对应的功能途径丰度提高；不同盐度处理下的样本按照功能途径进行聚类

Fig. 8 Heatmap showing the abundance (sqrt (x) transformed) distribution of potential functional pathways of gut bacterial communities in Sinonvacula constricta under three salinity stress

The color from blue to red represents an increase in the abundance of the corresponding functional pathway; samples under different salinity stress were clustered according to functional pathways

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表 1 基于Bray-Curtis 距离比较3种盐度处理下缢蛏肠道细菌群落的整体差异性

Tab. 1 Comparison of overall differences in gut bacterial communities among Sinonvacula constricta under three salinity stress based on Bray-Curtis distance

组别	N0		N15		L15		H15
组别	R	p	R	p	R	p	R	p
N0	−	−
N15	0.828	0.003	−	−
L15	0.960	0.002	0.317	0.036	−	−
H15	0.993	0.002	0.135	0.095	0.593	0.007	−	−
注：加粗的数值表示差异显著（p < 0.05）。

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表 2 基于非参数的多元置换方差分析不同盐度和胁迫时间对缢蛏肠道细菌群落的定量影响

Tab. 2 Quantitative effects of different salinity and stress time on the variations in gut bacterial community among Sinonvacula constricta based on nonparametric permutational multivariate analysis of variance

	自由度	平方和	均方差	F模型	R²	p
不同盐度	2	1.069	0.535	2.877	0.171	0.001
胁迫时间	1	1.473	1.473	7.929	0.235	0.001
残差	20	3.716	0.186		0.594
总计	23	6.259			1

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参考文献(43)

[1]	王劭雯. 皱纹盘鲍幼鲍对海水盐度的耐受性分析[D]. 青岛: 中国科学院海洋研究所, 2012. Wang Shaowen. Analysis of the toleration to different salinities in Haliotis discus hannai Ino[D]. Qingdao: Institute of Oceanology, Chinese Academy of Sciences, 2012.
[2]	Carregosa V, Figueira E, Gil A M, et al. Tolerance of Venerupis philippinarum to salinity: osmotic and metabolic aspects[J]. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2014, 171: 36−43.
[3]	蔡星媛, 张秀梅, 田璐, 等. 盐度胁迫对魁蚶稚贝血淋巴渗透压及鳃Na⁺/K⁺-ATP酶活力的影响[J]. 南方水产科学, 2015, 11(2): 12−19. Cai Xingyuan, Zhang Xiumei, Tian Lu, et al. Effect of salinity stress on hemolymph osmolality and gill Na⁺/K⁺-ATPase activity of juvenile ark shell ( Anadara broughtonii)[J]. South China Fisheries Science, 2015, 11(2): 12−19.
[4]	范超, 温子川, 霍忠明, 等. 盐度胁迫对不同发育时期菲律宾蛤仔生长和存活的影响[J]. 大连海洋大学学报, 2016, 31(5): 497−504. Fan Chao, Wen Zichuan, Huo Zhongming, et al. Influence of salinity stress on growth and survival of Manila clam Ruditapes philippinarum at various developmental stages[J]. Journal of Dalian Ocean University, 2016, 31(5): 497−504.
[5]	杨东敏, 张艳丽, 丁鉴锋, 等. 高温、低盐对菲律宾蛤仔免疫能力的影响[J]. 大连海洋大学学报, 2017, 32(3): 302−309. Yang Dongmin, Zhang Yanli, Ding Jianfeng, et al. Synergistic effects of high temperature and low salinity on immunity of Manila clam Ruditapes philippinarum[J]. Journal of Dalian Ocean University, 2017, 32(3): 302−309.
[6]	包锬, 刘一萌, 来琦芳, 等. 盐度胁迫对河蚬摄食率及鳃ATP酶活力变化研究[J]. 海洋渔业, 2021, 43(6): 671−679. doi: 10.3969/j.issn.1004-2490.2021.06.004 Bao Tan, Liu Yimeng, Lai Qifang, et al. Response of Corbicula fluminea's ingestion rate and branchial ATPase activity to salinity stress[J]. Marine Fisheries, 2021, 43(6): 671−679. doi: 10.3969/j.issn.1004-2490.2021.06.004
[7]	王怡, 胡婉彬, 李家祥, 等. 急性盐度胁迫对紫石房蛤( Saxidomus purpurata)鳃组织结构及4种酶活性的影响[J]. 中国农业科技导报, 2016, 18(5): 178−186. Wang Yi, Hu Wanbin, Li Jiaxiang, et al. Effects of acute salinity stress on gill structure and four enzyme activities in Saxidomus purpurata[J]. Journal of Agricultural Science and Technology, 2016, 18(5): 178−186.
[8]	Sun Fulin, Wang Chunzhong, Chen Xuelian. Bacterial community in Sinonovacula constricta intestine and its relationship with culture environment[J]. Applied Microbiology and Biotechnology, 2022, 106(13/16): 5211−5220.
[9]	Abid A, Davies S J, Waines P, et al. Dietary synbiotic application modulates Atlantic salmon ( Salmo salar) intestinal microbial communities and intestinal immunity[J]. Fish & Shellfish Immunology, 2013, 35(6): 1948−1956.
[10]	Cahenzli J, Köller Y, Wyss M, et al. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels[J]. Cell Host & Microbe, 2013, 14(5): 559−570.
[11]	Khan I, Huang Zubin, Liang Liangyue, et al. Ammonia stress influences intestinal histomorphology, immune status and microbiota of Chinese striped-neck turtle ( Mauremys sinensis)[J]. Ecotoxicology and Environmental Safety, 2021, 222: 112471. doi: 10.1016/j.ecoenv.2021.112471
[12]	张家松, 段亚飞, 张真真, 等. 对虾肠道微生物菌群的研究进展[J]. 南方水产科学, 2015, 11(6): 114−119. doi: 10.3969/j.issn.2095-0780.2015.06.016 Zhang Jiasong, Duan Yafei, Zhang Zhenzhen, et al. Research progress of intestinal microbial flora in shrimp[J]. South China Fisheries Science, 2015, 11(6): 114−119. doi: 10.3969/j.issn.2095-0780.2015.06.016
[13]	Eddy S D, Jones S H. Microbiology of summer flounder Paralichthys dentatus fingerling production at a marine fish hatchery[J]. Aquaculture, 2002, 211(1/4): 9−28.
[14]	Liu Jiajia, Wang Kai, Wang Yanting, et al. Strain-specific changes in the gut microbiota profiles of the white shrimp Litopenaeus vannamei in response to cold stress[J]. Aquaculture, 2019, 503: 357−366. doi: 10.1016/j.aquaculture.2019.01.026
[15]	田璐. 盐度对黄姑鱼生存生长、非特异性免疫及肠道菌群的影响[D]. 舟山: 浙江海洋大学, 2019. Tian Lu. Effects of salinity on growth, nonspecific immunity and micro-organism of Nibea albiflora[D]. Zhoushan: Zhejiang Ocean University, 2019.
[16]	Duan Yafei, Wang Yun, Liu Qingsong, et al. Changes in the intestine barrier function of Litopenaeus vannamei in response to pH stress[J]. Fish & Shellfish Immunology, 2019, 88: 142−149.
[17]	Zhang Tianxu, Zhang Yan, Xu Jiayun, et al. Toxic effects of ammonia on the intestine of the Asian clam ( Corbicula fluminea)[J]. Environmental Pollution, 2021, 287: 117617. doi: 10.1016/j.envpol.2021.117617
[18]	Dai Wenfang, Dong Yinghui, Ye Jing, et al. Gut microbiome composition likely affects the growth of razor clam Sinonovacula constricta[J]. Aquaculture, 2022, 550: 737847. doi: 10.1016/j.aquaculture.2021.737847
[19]	Pimentel Z T, Dufault-Thompson K, Russo K T, et al. Microbiome analysis reveals diversity and function of Mollicutes associated with the Eastern oyster, Crassostrea virginica[J]. mSphere, 2021, 6(3): e00227−21.
[20]	Li Yifeng, Yang Na, Liang Xiao, et al. Elevated seawater temperatures decrease microbial diversity in the gut of Mytilus coruscus[J]. Frontiers in Physiology, 2018, 9: 839. doi: 10.3389/fphys.2018.00839
[21]	Li Yifeng, Xu Jiakang, Chen Yanwen, et al. Characterization of gut microbiome in the mussel Mytilus galloprovincialis in response to thermal stress[J]. Frontiers in Physiology, 2019, 10: 1086. doi: 10.3389/fphys.2019.01086
[22]	林志华, 何琳, 董迎辉. 浙江滩涂贝类种业科技创新发展及展望[J]. 水产学报, 2023, 47(1): 019608. Lin Zhihua, He Lin, Dong Yinghui. Development and prospect for scientific and technological innovation of mudflat mollusk breeding industry in Zhejiang[J]. Journal of Fisheries of China, 2023, 47(1): 019608.
[23]	Cao Wei, Bi Siqi, Chi Changfeng, et al. Effects of high salinity stress on the survival, gill tissue, enzyme activity and free amino acid content in razor clam Sinonovacula constricta[J]. Frontiers in Marine Science, 2022, 9: 839614. doi: 10.3389/fmars.2022.839614
[24]	丁红兵, 李浩宇, 陈义华, 等. 高盐对缢蛏生长存活、Na⁺/K⁺-ATPase活性及能量代谢相关指标的影响[J]. 上海海洋大学学报, 2022, 31(4): 831−838. Ding Hongbing, Li Haoyu, Chen Yihua, et al. Effects of high salinity on growth and survival, Na⁺/K⁺-ATPase activity and energy metabolism related indexes of razor clam Sinonovacula constricta[J]. Journal of Shanghai Ocean University, 2022, 31(4): 831−838.
[25]	吕昊泽, 刘健, 陈锦辉, 等. 盐度对长江口3种滤食性贝类滤水率、摄食率、同化率的影响[J]. 海洋科学, 2016, 40(8): 10−17. Lü Haoze, Liu Jian, Chen Jinhui, et al. Effects of salinity on filtration, ingestion, and assimilation rates of three filter-feeding bivalves in the Yangtze River Estuary[J]. Marine Sciences, 2016, 40(8): 10−17.
[26]	Peng Maoxiao, Liu Xiaojun, Niu Donghong, et al. Survival, growth and physiology of marine bivalve ( Sinonovacula constricta) in long-term low-salt culture[J]. Scientific Reports, 2019, 9(1): 2819. doi: 10.1038/s41598-019-39205-2
[27]	李智, 彭茂潇, 叶博, 等. 急性低盐度对缢蛏存活率、Na⁺/K⁺-ATPase活性以及血淋巴细胞吞噬能力的影响[J]. 上海海洋大学学报, 2020, 29(4): 489−495. Li Zhi, Peng Maoxiao, Ye Bo, et al. Effects of acute low salinity on Sinonovacula constricta survival rate, Na⁺/K⁺-ATPase activity and phagocytosis of hemocytes[J]. Journal of Shanghai Ocean University, 2020, 29(4): 489−495.
[28]	Wei Yongjun, Ren Tianqi, Zhang Lei. Dix-seq: an integrated pipeline for fast amplicon data analysis[J/OL]. BioRxiv, 2020. doi: 10.1101/2020.05.11.089748
[29]	Magoč T, Salzberg S L. FLASH: fast length adjustment of short reads to improve genome assemblies[J]. Bioinformatics, 2011, 27(21): 2957−2963. doi: 10.1093/bioinformatics/btr507
[30]	Edgar R C. Search and clustering orders of magnitude faster than BLAST[J]. Bioinformatics, 2010, 26(19): 2460−2461. doi: 10.1093/bioinformatics/btq461
[31]	Caporaso J G, Bittinger K, Bushman F D, et al. PyNAST: a flexible tool for aligning sequences to a template alignment[J]. Bioinformatics, 2010, 26(2): 266−267. doi: 10.1093/bioinformatics/btp636
[32]	Stegen J C, Lin Xueju, Fredrickson J K, et al. Quantifying community assembly processes and identifying features that impose them[J]. The ISME Journal, 2013, 7(11): 2069−2079. doi: 10.1038/ismej.2013.93
[33]	Deng Ye, Jiang Y H, Yang Yunfeng, et al. Molecular ecological network analyses[J]. BMC Bioinformatics, 2012, 13(1): 113. doi: 10.1186/1471-2105-13-113
[34]	Wang Shidong, Li Xue, Zhang Muzi, et al. Ammonia stress disrupts intestinal microbial community and amino acid metabolism of juvenile yellow catfish ( Pelteobagrus fulvidraco)[J]. Ecotoxicology and Environmental Safety, 2021, 227: 112932. doi: 10.1016/j.ecoenv.2021.112932
[35]	Klase G, Lee S, Liang Song, et al. The microbiome and antibiotic resistance in integrated fishfarm water: implications of environmental public health[J]. Science of the Total Environment, 2019, 649: 1491−1501. doi: 10.1016/j.scitotenv.2018.08.288
[36]	王元, 周俊芳, 韦信贤, 等. 海水和淡水养殖凡纳滨对虾肠道和鳃的菌群结构分析[J]. 湖南农业大学学报(自然科学版), 2018, 44(2): 198−203. Wang Yuan, Zhou Junfang, Wei Xinxian, et al. Microbial community structure analysis of intestine and gill of Litopenaeus vannamei in seawater and freshwater[J]. Journal of Hunan Agricultural University (Natural Sciences), 2018, 44(2): 198−203.
[37]	Karimi E, Keller-Costa T, Slaby B M, et al. Genomic blueprints of sponge-prokaryote symbiosis are shared by low abundant and cultivatable Alphaproteobacteria[J]. Scientific Reports, 2019, 9(1): 1999. doi: 10.1038/s41598-019-38737-x
[38]	邹建威. 岩扇贝内脏团和肠道可培养微生物及其宏基因多样性分析[D]. 大连: 大连海洋大学, 2019. Zou Jianwei. Diversity analysis of culturable microorganisms and their macrogenes in rock scallop viscera and intestine[D]. Dalian: Dalian Ocean University, 2019.
[39]	King G M, Judd C, Kuske C R, et al. Analysis of stomach and gut microbiomes of the eastern oyster ( Crassostrea virginica) from coastal Louisiana, USA[J]. PLoS One, 2012, 7(12): e51475. doi: 10.1371/journal.pone.0051475
[40]	Gao Fangzhou, Liao Shaoan, Liu Shanshan, et al. The combination use of Candida tropicalis HH8 and Pseudomonas stutzeri LZX301 on nitrogen removal, biofloc formation and microbial communities in aquaculture[J]. Aquaculture, 2019, 500: 50−56. doi: 10.1016/j.aquaculture.2018.09.041
[41]	符振强, 董扬帆, 汤上上, 等. 低盐胁迫下饲料中添加α-硫辛酸对凡纳滨对虾生长、抗氧化能力及肠道健康的影响[J]. 动物营养学报, 2021, 33(9): 5203−5218. doi: 10.3969/j.issn.1006-267x.2021.09.040 Fu Zhenqiang, Dong Yangfan, Tang Shangshang, et al. Effects of dietary α-lipoic acid on growth, antioxidant capacity and intestinal health of Litopenaeus vannamei under low salinity stress[J]. Chinese Journal of Animal Nutrition, 2021, 33(9): 5203−5218. doi: 10.3969/j.issn.1006-267x.2021.09.040
[42]	Hou Dongwei, Zhou Renjun, Zeng Shenzheng, et al. Intestine bacterial community composition of shrimp varies under low- and high-salinity culture conditions[J]. Frontiers in Microbiology, 2020, 11: 589164. doi: 10.3389/fmicb.2020.589164
[43]	Krell T, Lacal J, Busch A, et al. Bacterial sensor kinases: diversity in the recognition of environmental signals[J]. Annual Review of Microbiology, 2010, 64(1): 539−559. doi: 10.1146/annurev.micro.112408.134054